Gene expression profile regulated by the HPV16 E7 oncoprotein and estradiol in cervical tissue

Virology

Volumn 447, Issue 1-2, 2013, Pages 155-165

  Cortés Malagón, Enoc M ^a,b   Bonilla Delgado, José ^b   Díaz Chávez, José ^c   Hidalgo Miranda, Alfredo ^d   Romero Cordoba, Sandra ^d   Üren, Aykut ^e   Çelik, Haydar ^e,i   McCormick, Matthew ^e   Munguía Moreno, José A ^a   Ibarra Sierra, Eloisa ^f   Escobar Herrera, Jaime ^a   Lambert, Paul F ^g   Mendoza Villanueva, Daniel ^h   Bermudez Cruz, Rosa M ^a   Gariglio, Patricio ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b HOSPITAL JUÁREZ DE MÉXICO   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d INSTITUTO NACIONAL DE MEDICINA GENÓMICA   (Mexico)

^e GEORGETOWN UNIVERSITY   (United States)

^f Research Laboratory Instituto Estatal de Cancerología   (Mexico)

^g UNIVERSITY OF WISCONSIN MADISON   (United States)

^h NATIONAL CANCER INSTITUTE   (United States)

ⁱ ERCIYES UNIVERSITY   (Turkey)

Author keywords

17 estradiol; Carcinogenesis; Cervix; HPV16 E7; K14E7; Microarrays

Indexed keywords

ESTRADIOL; PROTEIN E7;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNE RESPONSE; IMMUNOCHEMISTRY; IMMUNOFLUORESCENCE; KERATINOCYTE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRECANCER; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; UPREGULATION; UTERINE CERVIX CANCER;

17Β-ESTRADIOL; CARCINOGENESIS; CERVIX; HPV16 E7; K14E7; MICROARRAYS;

ANIMALS; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; MICE; MICE, TRANSGENIC; PAPILLOMAVIRUS E7 PROTEINS;

EID: 84884944259     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.08.036     Document Type: Article

References (76)

1. Agarwal R., D'Souza T., Morin P.J. Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res. 2005, 65(16):7378-7385.
2. Al-Tahhan M.A., Etewa R.L., El Behery M.M. Association between circulating interleukin-1 beta (IL-1beta) levels and IL-1beta C-511T polymorphism with cervical cancer risk in Egyptian women. Mol. Cell. Biochem. 2011, 353(1-2):159-165.
3. Al Moustafa A.E., Alaoui-Jamali M.A., Batist G., Hernandez-Perez M., Serruya C., Alpert L., Black M.J., Sladek R., Foulkes W.D. Identification of genes associated with head and neck carcinogenesis by cDNA microarray comparison between matched primary normal epithelial and squamous carcinoma cells. Oncogene 2002, 21(17):2634-2640.
4. Arbeit J.M., Howley P.M., Hanahan D. Chronic estrogen-induced cervical and vaginal squamous carcinogenesis in human papillomavirus type 16 transgenic mice. Proc. Nat. Acad. Sci. U.S.A. 1996, 93(7):2930-2935.
5. Balsitis S., Dick F., Dyson N., Lambert P.F. Critical roles for non-pRb targets of human papillomavirus type 16 E7 in cervical carcinogenesis. Cancer Res. 2006, 66(19):9393-9400.
6. Bando M., Hiroshima Y., Kataoka M., Shinohara Y., Herzberg M.C., Ross K.F., Nagata T., Kido J. Interleukin-1alpha regulates antimicrobial peptide expression in human keratinocytes. Immunol. Cell Biol. 2007, 85(7):532-537.
7. Brake T., Lambert P.F. Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc. Nat. Acad. Sci. U.S.A. 2005, 102(7):2490-2495.
8. Branca M., Ciotti M., Giorgi C., Santini D., Di Bonito L., Costa S., Benedetto A., Bonifacio D., Di Bonito P., Paba P., Accardi L., Syrjanen S., Favalli C., Syrjanen K. Up-regulation of proliferating cell nuclear antigen (PCNA) is closely associated with high-risk human papillomavirus (HPV) and progression of cervical intraepithelial neoplasia (CIN), but does not predict disease outcome in cervical cancer. Eur. J. Obstet. Gynaecol. Reprod. Biol. 2007, 130(2):223-231.
9. Brisson J., Morin C., Fortier M., Roy M., Bouchard C., Leclerc J., Christen A., Guimont C., Penault F., Meisels A. Risk factors for cervical intraepithelial neoplasia: differences between low- and high-grade lesions. Am. J. Epidemiol. 1994, 140(8):700-710.
10. Castrilli G., Tatone D., Diodoro M.G., Rosini S., Piantelli M., Musiani P. Interleukin 1alpha and interleukin 6 promote the in vitro growth of both normal and neoplastic human cervical epithelial cells. Br. J. Cancer 1997, 75(6):855-859.
11. Chen Y., Cairns R., Papandreou I., Koong A., Denko N.C. Oxygen consumption can regulate the growth of tumors, a new perspective on the Warburg effect. PLoS One 2009, 4(9):e7033.
12. Cheng R.J., Deng W.G., Niu C.B., Li Y.Y., Fu Y. Expression of macrophage migration inhibitory factor and CD74 in cervical squamous cell carcinoma. Int. J. Gynecol. Cancer 2011, 21(6):1004-1012.
13. Cheng W.L., Wang C.S., Huang Y.H., Tsai M.M., Liang Y., Lin K.H. Overexpression of CXCL1 and its receptor CXCR2 promote tumor invasion in gastric cancer. Ann. Oncol. 2011, 22(10):2267-2276.
14. Choi Y.W., Kim Y.W., Bae S.M., Kwak S.Y., Chun H.J., Tong S.Y., Lee H.N., Shin J.C., Kim K.T., Kim Y.J., Ahn W.S. Identification of differentially expressed genes using annealing control primer-based GeneFishing in human squamous cell cervical carcinoma. Clin. Oncol. (R. Coll. Radiol.) 2007, 19(5):308-318.
15. Chung S.H., Shin M.K., Korach K.S., Lambert P.F. Requirement for stromal estrogen receptor alpha in cervical neoplasia. Horm. Cancer 2013, 4(1):50-59.
16. Chung S.H., Wiedmeyer K., Shai A., Korach K.S., Lambert P.F. Requirement for estrogen receptor alpha in a mouse model for human papillomavirus-associated cervical cancer. Cancer Res. 2008, 68(23):9928-9934.
17. Darnell G.A., Schroder W.A., Antalis T.M., Lambley E., Major L., Gardner J., Birrell G., Cid-Arregui A., Suhrbier A. Human papillomavirus E7 requires the protease calpain to degrade the retinoblastoma protein. J. Biol. Chem. 2007, 282(52):37492-37500.
18. del Pino M., Garcia S., Fuste V., Alonso I., Fuste P., Torne A., Ordi J. Value of p16(INK4a) as a marker of progression/regression in cervical intraepithelial neoplasia grade 1. Am. J. Obstet. Gynecol. 2009, 201(5). (488 e1-7).
19. Dray M., Russell P., Dalrymple C., Wallman N., Angus G., Leong A., Carter J., Cheerala B. p16(INK4a) as a complementary marker of high-grade intraepithelial lesions of the uterine cervix. I: Experience with squamous lesions in 189 consecutive cervical biopsies. Pathology 2005, 37(2):112-124.
20. Elson D.A., Riley R.R., Lacey A., Thordarson G., Talamantes F.J., Arbeit J.M. Sensitivity of the cervical transformation zone to estrogen-induced squamous carcinogenesis. Cancer Res. 2000, 60(5):1267-1275.
21. Flores E.R., Allen-Hoffmann B.L., Lee D., Lambert P.F. The human papillomavirus type 16 E7 oncogene is required for the productive stage of the viral life cycle. J. Virol. 2000, 74(14):6622-6631.
22. Gariglio P., Gutierrez J., Cortes E., Vazquez J. The role of retinoid deficiency and estrogens as cofactors in cervical cancer. Arch. Med. Res. 2009, 40(6):449-465.
23. Ghittoni R., Accardi R., Hasan U., Gheit T., Sylla B., Tommasino M. The biological properties of E6 and E7 oncoproteins from human papillomaviruses. Virus Genes 2010, 40(1):1-13.
24. Gius D., Funk M.C., Chuang E.Y., Feng S., Huettner P.C., Nguyen L., Bradbury C.M., Mishra M., Gao S., Buttin B.M., Cohn D.E., Powell M.A., Horowitz N.S., Whitcomb B.P., Rader J.S. Profiling microdissected epithelium and stroma to model genomic signatures for cervical carcinogenesis accommodating for covariates. Cancer Res. 2007, 67(15):7113-7123.
25. Gruber C.J., Tschugguel W., Schneeberger C., Huber J.C. Production and actions of estrogens. N. Engl. J. Med. 2002, 346(5):340-352.
26. Gyongyosi E., Szalmas A., Ferenczi A., Konya J., Gergely L., Veress G. Effects of human papillomavirus (HPV) type 16 oncoproteins on the expression of involucrin in human keratinocytes. Virol. J. 2012, 9:36.
27. Halbert C.L., Demers G.W., Galloway D.A. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 1991, 65(1):473-478.
28. Herbsleb M., Knudsen U.B., Orntoft T.F., Bichel P., Norrild B., Knudsen A., Mogensen O. Telomerase activity, MIB-1, PCNA, HPV 16 and p53 as diagnostic markers for cervical intraepithelial neoplasia. APMIS: Acta Pathol. Microbiol. Immunol. Scand. 2001, 109:607-617.
29. Hiratsuka S., Watanabe A., Aburatani H., Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 2006, 8(12):1369-1375.
30. Ibarra Sierra E., Diaz Chavez J., Cortes-Malagon E.M., Uribe-Figueroa L., Hidalgo-Miranda A., Lambert P.F., Gariglio P. Differential gene expression between skin and cervix induced by the E7 oncoprotein in a transgenic mouse model. Virology 2012, 433(2):337-345.
31. Ichikawa M., Williams R., Wang L., Vogl T., Srikrishna G. S100A8/A9 activate key genes and pathways in colon tumor progression. Mol. Cancer Res. 2011, 9(2):133-148.
32. Jabbar S.F., Abrams L., Glick A., Lambert P.F. Persistence of high-grade cervical dysplasia and cervical cancer requires the continuous expression of the human papillomavirus type 16 E7 oncogene. Cancer Res. 2009, 69(10):4407-4414.
33. Kallberg E., Vogl T., Liberg D., Olsson A., Bjork P., Wikstrom P., Bergh A., Roth J., Ivars F., Leanderson T. S100A9 interaction with TLR4 promotes tumor growth. PLoS One 2012, 7(3):e34207.
34. Karim R., Jordanova E.S., Piersma S.J., Kenter G.G., Chen L., Boer J.M., Melief C.J., van der Burg S.H. Tumor-expressed B7-H1 and B7-DC in relation to PD-1+ T-cell infiltration and survival of patients with cervical carcinoma. Clin. Cancer Res. 2009, 15(20):6341-6347.
35. Kominsky S.L., Argani P., Korz D., Evron E., Raman V., Garrett E., Rein A., Sauter G., Kallioniemi O.P., Sukumar S. Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast. Oncogene 2003, 22(13):2021-2033.
36. Kurshumliu F., Thorns C., Gashi-Luci L. p16INK4A in routine practice as a marker of cervical epithelial neoplasia. Gynecol. Oncol. 2009, 115(1):127-131.
37. Lago C.U., Nowinski S.M., Rundhaug J.E., Pfeiffer M.E., Kiguchi K., Hirasaka K., Yang X., Abramson E.M., Bratton S.B., Rho O., Colavitti R., Kenaston M.A., Nikawa T., Trempus C., Digiovanni J., Fischer S.M., Mills E.M. Mitochondrial respiratory uncoupling promotes keratinocyte differentiation and blocks skin carcinogenesis. Oncogene 2012, 31(44):4725-4731.
38. Lee S.Y., Jeon H.M., Ju M.K., Kim C.H., Yoon G., Han S.I., Park H.G., Kang H.S. Wnt/Snail signaling regulates cytochrome C oxidase and glucose metabolism. Cancer Res. 2012, 72(14):3607-3617.
39. Lei Z.B., Fu X.J., Lu Z.T., Wang B.C., Liu X.L., You N.Z. Effect of estradiol on chemokine receptor CXCR2 expression in rats: implications for atherosclerosis. Acta Pharmacol. Sin. 2003, 24(7):670-674.
40. Li C., Li S., Jia C., Yang L., Song Z., Wang Y. Low concentration of S100A8/9 promotes angiogenesis-related activity of vascular endothelial cells: bridges among inflammation, angiogenesis, and tumorigenesis?. Mediators Inflamm. 2012, 2012:248574.
41. Long H., Crean C.D., Lee W.H., Cummings O.W., Gabig T.G. Expression of Clostridium perfringens enterotoxin receptors claudin-3 and claudin-4 in prostate cancer epithelium. Cancer Res. 2001, 61(21):7878-7881.
42. Mailloux R.J., Harper M.E. Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radical Biol. Med. 2011, 51(6):1106-1115.
43. Manavi M., Hudelist G., Fink-Retter A., Gschwandtler-Kaulich D., Pischinger K., Czerwenka K. Gene profiling in Pap-cell smears of high-risk human papillomavirus-positive squamous cervical carcinoma. Gynecol. Oncol. 2007, 105(2):418-426.
44. Markowitz J., Carson W.E. Review of S100A9 biology and its role in cancer. Biochim. Biophys. Acta 2013, 1835(1):100-109.
45. McLaughlin-Drubin M.E., Munger K. The human papillomavirus E7 oncoprotein. Virology 2009, 384(2):335-344.
46. Middleton K., Peh W., Southern S., Griffin H., Sotlar K., Nakahara T., El-Sherif A., Morris L., Seth R., Hibma M., Jenkins D., Lambert P., Coleman N., Doorbar J. Organization of human papillomavirus productive cycle during neoplastic progression provides a basis for selection of diagnostic markers. J. Virol. 2003, 77(19):10186-10201.
47. Missaoui N., Trabelsi A., Hmissa S., Fontaniere B., Yacoubi M.T., Mokni M., Korbi S., Frappart L. p16INK4A overexpression in precancerous and cancerous lesions of the uterine cervix in Tunisian women. Pathol. Res. Pract. 2010, 206(8):550-555.
48. Moody C.A., Laimins L.A. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 2010, 10(8):550-560.
49. Moreno V., Bosch F.X., Munoz N., Meijer C.J., Shah K.V., Walboomers J.M., Herrero R., Franceschi S. Effect of oral contraceptives on risk of cervical cancer in women with human papillomavirus infection: the IARC multicentric case-control study. Lancet 2002, 359(9312):1085-1092.
50. Morin P.J. Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res. 2005, 65(21):9603-9606.
51. Munger K., Baldwin A., Edwards K.M., Hayakawa H., Nguyen C.L., Owens M., Grace M., Huh K. Mechanisms of human papillomavirus-induced oncogenesis. J. Virol. 2004, 78(21):11451-11460.
52. Nichols L.S., Ashfaq R., Iacobuzio-Donahue C.A. Claudin 4 protein expression in primary and metastatic pancreatic cancer: support for use as a therapeutic target. Am. J. Clin. Pathol. 2004, 121(2):226-230.
53. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., Gustafsson J.A. Mechanisms of estrogen action. Physiol. Rev. 2001, 81(4):1535-1565.
54. Panse J., Friedrichs K., Marx A., Hildebrandt Y., Luetkens T., Barrels K., Horn C., Stahl T., Cao Y., Milde-Langosch K., Niendorf A., Kroger N., Wenzel S., Leuwer R., Bokemeyer C., Hegewisch-Becker S., Atanackovic D. Chemokine CXCL13 is overexpressed in the tumour tissue and in the peripheral blood of breast cancer patients. Br. J. Cancer 2008, 99(6):930-938.
55. Polan M.L., Daniele A., Kuo A. Gonadal steroids modulate human monocyte interleukin-1 (IL-1) activity. Fertil. Steril. 1988, 49(6):964-968.
56. Qin F., Song Y., Li Z., Zhao L., Zhang Y., Geng L. S100A8/A9 induces apoptosis and inhibits metastasis of CasKi human cervical cancer cells. Pathol. Oncol. Res. 2010, 16(3):353-360.
57. Riley R.R., Duensing S., Brake T., Munger K., Lambert P.F., Arbeit J.M. Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis. Cancer Res. 2003, 63(16):4862-4871.
58. Riva M., He Z., Kallberg E., Ivars F., Leanderson T. Human S100A9 protein is stabilized by inflammatory stimuli via the formation of proteolytically-resistant homodimers. PLoS One 2013, 8(4):e61832.
59. Ruh M.F., Bi Y., D'Alonzo R., Bellone C.J. Effect of estrogens on IL-1beta promoter activity. J. Steroid. Biochem. Mol. Biol. 1998, 66(4):203-210.
60. Salazar E.L., Sojo-Aranda I., Lopez R., Salcedo M. The evidence for an etiological relationship between oral contraceptive use and dysplastic change in cervical tissue. Gynecol. Endocrinol.: Off. J. Int. Soc. Gynecol. Endocrinol. 2001, 15(1):23-28.
61. Santin A.D., Zhan F., Bignotti E., Siegel E.R., Cane S., Bellone S., Palmieri M., Anfossi S., Thomas M., Burnett A., Kay H.H., Roman J.J., O'Brien T.J., Tian E., Cannon M.J., Shaughnessy J., Pecorelli S. Gene expression profiles of primary HPV16- and HPV18-infected early stage cervical cancers and normal cervical epithelium: identification of novel candidate molecular markers for cervical cancer diagnosis and therapy. Virology 2005, 331(2):269-291.
62. Seder C.W., Hartojo W., Lin L., Silvers A.L., Wang Z., Thomas D.G., Giordano T.J., Chen G., Chang A.C., Orringer M.B., Beer D.G. Upregulated INHBA expression may promote cell proliferation and is associated with poor survival in lung adenocarcinoma. Neoplasia 2009, 11(4):388-396.
63. Shai, A., Brake, T., Somoza, C., Lambert, P.F., 2007. The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res. 67 (4), 1626-1635.
64. Shang X., Lin X., Alvarez E., Manorek G., Howell S.B. Tight junction proteins claudin-3 and claudin-4 control tumor growth and metastases. Neoplasia 2012, 14(10):974-985.
65. Silva T.A., Ribeiro F.L., Oliveira-Neto H.H., Watanabe S., Alencar Rde C., Fukada S.Y., Cunha F.Q., Leles C.R., Mendonca E.F., Batista A.C. Dual role of CCL3/CCR1 in oral squamous cell carcinoma: implications in tumor metastasis and local host defense. Oncol. Rep. 2007, 18(5):1107-1113.
66. Sobel G., Paska C., Szabo I., Kiss A., Kadar A., Schaff Z. Increased expression of claudins in cervical squamous intraepithelial neoplasia and invasive carcinoma. Hum. Pathol. 2005, 36(2):162-169.
67. Srikrishna G. S100A8 and S100A9: new insights into their roles in malignancy. J. Innate Immun. 2012, 4(1):31-40.
68. Stygar D., Masironi B., Eriksson H., Sahlin L. Studies on estrogen receptor (ER) alpha and beta responses on gene regulation in peripheral blood leukocytes in vivo using selective ER agonists. J. Endocrinol. 2007, 194(1):101-119.
69. Tsukita S., Furuse M. Claudin-based barrier in simple and stratified cellular sheets. Curr. Opin. Cell. Biol. 2002, 14(5):531-536.
70. Tugizov S., Berline J., Herrera R., Penaranda M.E., Nakagawa M., Palefsky J. Inhibition of human papillomavirus type 16 E7 phosphorylation by the S100 MRP-8/14 protein complex. J. Virol. 2005, 79(2):1099-1112.
71. Vendrell J.A., Ghayad S., Ben-Larbi S., Dumontet C., Mechti N., Cohen P.A. A20/TNFAIP3, a new estrogen-regulated gene that confers tamoxifen resistance in breast cancer cells. Oncogene 2007, 26(32):4656-4667.
72. Wang Q., Wen Y.G., Li D.P., Xia J., Zhou C.Z., Yan D.W., Tang H.M., Peng Z.H. Upregulated INHBA expression is associated with poor survival in gastric cancer. Med. Oncol. 2012, 29(1):77-83.
73. Webb P.G., Spillman M.A., Baumgartner H.K. Claudins play a role in normal and tumor cell motility. BMC Cell Biol. 2013, 14:19.
74. Zhai Y., Kuick R., Nan B., Ota I., Weiss S.J., Trimble C.L., Fearon E.R., Cho K.R. Gene expression analysis of preinvasive and invasive cervical squamous cell carcinomas identifies HOXC10 as a key mediator of invasion. Cancer Res. 2007, 67(21):10163-10172.
75. Zhu X., Jin L., Zou S., Shen Q., Jiang W., Lin W. Immunohistochemical expression of RAGE and its ligand (S100A9) in cervical lesions. Cell Biochem. Biophys 2013.
76. Zhu X., Lv J., Yu L., Wu J., Zou S., Jiang S. Proteomic identification of differentially-expressed proteins in squamous cervical cancer. Gynecol. Oncol. 2009, 112(1):248-256.